Research Article
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Hazelnut-enriched diet effectively increases lipoproteins' resistance to oxidation in hypercholesterolemic subjects

Year 2023, Volume: 9 Issue: 3, 201 - 211, 05.07.2023
https://doi.org/10.3153/FH23019

Abstract

Oxidative modifications of lipoproteins are crucial in the early stages of cardiovascular diseases (CVD) like hypercholesterolemia. The major aim is to determine the effects of hazelnut consumption on the resistance of low- and high-density lipoproteins to oxidation in hypercholesterolemic subjects. Fifteen hypercholesterolemic subjects (13 men, 2 women) who did not require drug treatment according to the National Cholesterol Education Program Adult Treatment Panel III criteria and had serum levels of TC˃200 mg/dL were included in the study. This study was designed as a dual control sandwich model intervention with a single group, isoenergetic three periods. The periods were; Control Diet I (30 days), Hazelnut-Enriched Diet (30 days), and Control Diet II (30 days). The susceptibility of LDL and HDL to copper-mediated oxidation was determined spectrophotometrically by following conjugated diene formation. The resistance of lipoproteins, mainly LDL, was increased by hazelnut consumption. It can be concluded that a hazelnut-enriched diet had protective effects against lipoprotein oxidation in hypercholesterolemic subjects. These changes may play important roles in reducing the development of the atherosclerotic process.

Supporting Institution

Karadeniz Technical University Scientific Research Projects Coordination Unit.

Thanks

The authors are thankful to Filiz Kansız, who works as a dietician at the Farabi Hospital for collecting of nutritional data.

References

  • Akhlaghi, M., Ghobadi, S., Zare, M., Foshati, S. (2020). Effect of nuts on energy intake, hunger, and fullness, a systematic review and meta-analysis of randomized clinical trials. Critical Reviews in Food Science and Nutrition, 60(1), 84–93. https://doi.org/10.1080/10408398.2018.1514486
  • Balaban Yucesan, F., Orem, A., Vanizor Kural, B., Orem, C., Turan, I. (2010). Hazelnut consumption decreases the susceptibility of LDL to oxidation, plasma oxidized LDL level and increases the ratio of large/small LDL in normolipidemic healthy subjects. Anadolu Kardiyoloji Dergisi/The Anatolian Journal of Cardiology, 10, 28-35. https://doi.org/10.5152/akd.2010.007
  • Borén, J., Chapman, M. J., Krauss, R. M., Packard, C. J., Bentzon, J. F., Binder, C. J., et al. (2020). Low-density lipoproteins cause atherosclerotic cardiovascular disease: pathophysiological, genetic, and therapeutic insights: a consensus statement from the European Atherosclerosis Society Consensus Panel. European Heart Journal, 41(24), 2313–2330. https://doi.org/10.1093/eurheartj/ehz962
  • Brown, R., Ware, L., Tey, S. L. (2022). Effects of Hazelnut Consumption on Cardiometabolic Risk Factors and Acceptance: A Systematic Review. In International Journal of Environmental Research and Public Health, 19(5), 2880. https://doi.org/10.3390/ijerph19052880
  • Deon, V., del Bo’, C., Guaraldi, F., Abello, F., Belviso, S., Porrini, M., Riso, P., Guardamagna, O. (2018). Effect of hazelnut on serum lipid profile and fatty acid composition of erythrocyte phospholipids in children and adolescents with primary hyperlipidemia: A randomized controlled trial. Clinical Nutrition, 37(4), 1193–1201. https://doi.org/10.1016/j.clnu.2017.05.022
  • Durak, I., Koksal, I., Kacmaz, M., Buyukkocak, S., Cimen, B.M.Y., Ozturk, H.S. (1999). Hazelnut supplementation enhances plasma antioxidant potential and lowers plasma cholesterol levels. Clinica Chimica Acta, 284, 113–115. https://doi.org/10.1016/S0009-8981(99)00066-2
  • Edwards, K., Kwaw, I., Matud, J., Kurtz, I. (1999). Effect of Pistachio Nuts on Serum Lipid Levels in Patients with Moderate Hypercholesterolemia. Journal of the American College of Nutrition, 18(3), 229-232. https://doi.org/10.1080/07315724.1999.10718856
  • Fraser, G.E. (2000). Nut consumption, lipids, and risk of a coronary event. Asia Pacific Journal of Clinical Nutrition, 111, 11-15. https://doi.org/10.1046/j.1440-6047.2000.00181.x
  • Garner, B., Waldeck, A.R., Witting, P.K., Rye, K.-A., Stocker, R. (1998). Oxidation of high-density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. Journal of Biological Chemistry, 273 (13), 6088-6095. https://doi.org/10.1074/jbc.273.11.6088
  • Gießauf, A., Steiner, E., Esterbauer, H. (1995). Early destruction of tryptophan residues of apolipoprotein B is a vitamin E-independent process during copper-mediated oxidation of LDL. Biochimica et Biophysica Acta (BBA)/Lipids and Lipid Metabolism, 1256(2), 221–232. https://doi.org/10.1016/0005-2760(95)00024-7
  • Grundy, S.M., Cleeman, J.I., Bairey Merz, C.N., Brewer, H.B., Clark, L. T., Hunninghake, D.B., Pasternak, R.C., Smith, S.C., Stone, N.J. (2004). Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation,110, 227-239. https://doi.org/10.1161/01.CIR.0000133317.49796.0E
  • Hargrove, R.L., Etherton, T.D., Pearson, T.A., Harrison, E.H., Kris-Etherton, P.M. (2001). Low fat and high monounsaturated fat diets decrease human low density lipoprotein oxidative susceptibility in vitro. The Journal of Nutrition, 131(6), 1758–1763. https://doi.org/10.1093/jn/131.6.1758
  • Hasselwander, O., McEneny, J., McMaster, D., Fogarty, D.G., Nicholls, D.P., Maxwell, A.P., Young, I.S. (1999). HDL composition and HDL antioxidant capacity in patients on regular haemodialysis. Atherosclerosis, 143(1), 125-133. https://doi.org/10.1016/S0021-9150(98)00286-X
  • Jiang, R., Jacobs, D.R., Mayer-Davis, E., Szklo, M., Herrington, D., Jenny, N.S., Kronmal, R., Barr, R.G. (2006). Nut and seed consumption and inflammatory markers in the Multi-Ethnic Study of Atherosclerosis. American Journal of Epidemiology,163(3), 222-231. https://doi.org/10.1093/aje/kwj033
  • Kocyigit, A., Koylu, A.A., Keles, H. (2006). Effects of pistachio nuts consumption on plasma lipid profile and oxidative status in healthy volunteers. Nutrition, Metabolism and Cardiovascular Diseases, 16(3), 202–209. https://doi.org/10.1016/j.numecd.2005.08.004
  • Oliver H., Lowry, Nira J., Rosebrough A., Lewis Farr, Rose Randall (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry. 193 (1) 265-275. https://doi.org/10.1021/jf1005935. MercanlIgil, S.M., Arslan, P., Alasalvar, C., Okut, E., Akgül, E., PInar, A., Geyik, P.Ö., Tokgözoǧlu, L., Shahidi, F. (2007). Effects of hazelnut-enriched diet on plasma cholesterol and lipoprotein profiles in hypercholesterolemic adult men. European Journal of Clinical Nutrition. 61, 212-220. https://doi.org/10.1038/sj.ejcn.1602518
  • Mukuddem-Petersen, J., Oosthuizen, W., Jerling, J. C. (2005). A systematic review of the effects of nuts on blood lipid profiles in humans. The Journal of Nutrition, 135(9), 2082–2089. https://doi.org/10.1093/jn/135.9.2082
  • Nag, T., Ghosh, A. (2013). Cardiovascular disease risk factors in Asian Indian population: A systematic review. Journal of Cardiovascular Disease Research, 4 (4), 222-228. https://doi.org/10.1016/j.jcdr.2014.01.004
  • Negre-Salvayre, A., Dousset, N., Ferretti, G., Bacchetti, T., Curatola, G., Salvayre, R. (2006). Antioxidant and cytoprotective properties of high-density lipoproteins in vascular cells. Free Radical Biology and Medicine, 41(7), 1031-1040. https://doi.org/10.1016/j.freeradbiomed.2006.07.006
  • Nicholls, S.J., Nelson, A. J. (2019). HDL and cardiovascular disease. Pathology, 51(2), 142–147. https://doi.org/10.1016/j.pathol.2018.10.017
  • Norata, G.D., Pirillo, A., Catapano, A.L. (2006). Modified HDL: Biological and physiopathological consequences. Nutrition, Metabolism and Cardiovascular Diseases, 16(5), 371-386. https://doi.org/10.1016/j.numecd.2006.01.012
  • Öngün Yilmaz, H., Özyildirim, B. (2019). Evaluation of the effects of raisins and hazelnuts added to the diet on lipid profiles and anthropometric measurements in women with hyperlipidemia. Bezmialem Science, 7(4), 294–306. https://doi.org/10.14235/bas.galenos.2019.2969
  • Orem, A., Yucesan, F. B., Orem, C., Akcan, B., Kural, B. V., Alasalvar, C., Shahidi, F. (2013). Hazelnut-enriched diet improves cardiovascular risk biomarkers beyond a lipid-lowering effect in hypercholesterolemic subjects. Journal of Clinical Lipidology, 7(2), 123-131. https://doi.org/10.1016/j.jacl.2012.10.005
  • Proudfoot, J. M., Croft, K. D., Puddey, I. B., Beilin, L. J. (1997). The role of copper reduction by α-tocopherol in low-density lipoprotein oxidation. Free Radical Biology and Medicine, 23(5), 720-728. https://doi.org/10.1016/S0891-5849(97)00015-4
  • Puhl, H., Waeg, G., Esterbauer, H. (1994). Methods to determine oxidation of low-density lipoproteins. Methods in Enzymology, 233, 425-441 https://doi.org/10.1016/S0076-6879(94)33049-2
  • Renzo, L. Di, Cioccoloni, G., Bernardini, S., Abenavoli, L., Aiello, V., Marchetti, M., Cammarano, A., Alipourfard, I., Ceravolo, I., Gratteri, S. (2019). A hazelnut-enriched diet modulates oxidative stress and inflammation gene expression without weight gain. Oxidative Medicine and Cellular Longevity, 2019, 1-11. https://doi.org/10.1155/2019/4683723
  • Ros, E., Nunez, I., Perez-Heras, A., Serra, M., Gilabert, R., Casals, E., Deulofeu, R. (2004). A walnut diet improves endothelial function in hypercholesterolemic subjects: a randomized crossover trial. Circulation, 109(13), 1609-1614. https://doi.org/10.1161/01.CIR.0000124477.91474.FF
  • Garcı´a-L., I Megias R., J Salas S. (2003). Nut consumption and body weight. Am. J. Clinical Nutrition. 57(1), 8-11. https://doi.org/10.1038/sj.ejcn.1601802
  • Sclavons, M.M., Cordonnier, C.M., Mailleux, P.M., Heller, F.R., Desager, J.P., Harvengt, C.M. (1985). Fast separation of the three main plasma lipoprotein classes by ultracentrifugation using vertical rotor and multiple discontinuous density gradient. Clinica Chimica Acta, 153(2), 125-135. https://doi.org/10.1016/0009-8981(85)90163-9
  • Segovia-Siapco, G., Sabaté, J. (2018). Health and sustainability outcomes of vegetarian dietary patterns: a revisit of the EPIC-Oxford and the Adventist Health Study-2 cohorts. European Journal of Clinical Nutrition, 72, 60–70. https://doi.org/10.1038/s41430-018-0310-z
  • Singh, U.N., Kumar, S., Dhakal, S. (2017). Study of Oxidative Stress in Hypercholesterolemia. International Journal of Contemporary Medical Research, 4(5), 2454–7379.
  • Spiller, G.A., Gates, J.E., Cragen, L.N., Bruce, B., Jenkins, D.A.J., Bosello, O. (1998). Nuts and plasma lipids: An almond-based diet lowers LDL-C while preserving HDL-C. Journal of the American College of Nutrition, 17(3)-285-290. https://doi.org/10.1080/07315724.1998.10718761
  • Steinberg, D., Parthasarathy, S., Carew, T.E., Khoo, J.C., Witztum, J.L. (1989). Beyond cholesterol: Modifications of low-density lipoprotein that increase its atherogenicity. New England Journal of Medicine, 94, 215-244. Tey, S.L., Brown, R.C., Chisholm, A.W., Delahunty, C.M., Gray, A.R., Williams, S.M. (2011). Effects of different forms of hazelnuts on blood lipids and α-tocopherol concentrations in mildly hypercholesterolemic individuals. European Journal of Clinical Nutrition, 65, 117-124. https://doi.org/10.1038/ejcn.2010.200
  • Vanizor Kural, B., Örem, A., Çimşit, G., Yandı, Y.E., Calapoǧlu, M. (2003). Evaluation of the atherogenic tendency of lipids and lipoprotein content and their relationships with oxidant–antioxidant system in patients with psoriasis. Clinica Chimica Act, 328(1), 71-82. https://doi.org/https://doi.org/10.1016/S0009-8981(02)00373-X
  • Winklhofer-Roob, B.M., Faustmann, G., Roob, J.M. (2017). Low-density lipoprotein oxidation biomarkers in human health and disease and effects of bioactive compounds. Free Radical Biology and Medicine, 111, 38–86. https://doi.org/10.1016/j.freeradbiomed.2017.04.345
  • Zabłocka-Słowińska, K., Płaczkowska, S., Skórska, K., Prescha, A., Pawełczyk, K., Porębska, I., Kosacka, M., Grajeta, H. (2019). Oxidative stress in lung cancer patients is associated with altered serum markers of lipid metabolism. PLoS ONE, 14(4), 1–20. https://doi.org/10.1371/journal.pone.0215246
Year 2023, Volume: 9 Issue: 3, 201 - 211, 05.07.2023
https://doi.org/10.3153/FH23019

Abstract

References

  • Akhlaghi, M., Ghobadi, S., Zare, M., Foshati, S. (2020). Effect of nuts on energy intake, hunger, and fullness, a systematic review and meta-analysis of randomized clinical trials. Critical Reviews in Food Science and Nutrition, 60(1), 84–93. https://doi.org/10.1080/10408398.2018.1514486
  • Balaban Yucesan, F., Orem, A., Vanizor Kural, B., Orem, C., Turan, I. (2010). Hazelnut consumption decreases the susceptibility of LDL to oxidation, plasma oxidized LDL level and increases the ratio of large/small LDL in normolipidemic healthy subjects. Anadolu Kardiyoloji Dergisi/The Anatolian Journal of Cardiology, 10, 28-35. https://doi.org/10.5152/akd.2010.007
  • Borén, J., Chapman, M. J., Krauss, R. M., Packard, C. J., Bentzon, J. F., Binder, C. J., et al. (2020). Low-density lipoproteins cause atherosclerotic cardiovascular disease: pathophysiological, genetic, and therapeutic insights: a consensus statement from the European Atherosclerosis Society Consensus Panel. European Heart Journal, 41(24), 2313–2330. https://doi.org/10.1093/eurheartj/ehz962
  • Brown, R., Ware, L., Tey, S. L. (2022). Effects of Hazelnut Consumption on Cardiometabolic Risk Factors and Acceptance: A Systematic Review. In International Journal of Environmental Research and Public Health, 19(5), 2880. https://doi.org/10.3390/ijerph19052880
  • Deon, V., del Bo’, C., Guaraldi, F., Abello, F., Belviso, S., Porrini, M., Riso, P., Guardamagna, O. (2018). Effect of hazelnut on serum lipid profile and fatty acid composition of erythrocyte phospholipids in children and adolescents with primary hyperlipidemia: A randomized controlled trial. Clinical Nutrition, 37(4), 1193–1201. https://doi.org/10.1016/j.clnu.2017.05.022
  • Durak, I., Koksal, I., Kacmaz, M., Buyukkocak, S., Cimen, B.M.Y., Ozturk, H.S. (1999). Hazelnut supplementation enhances plasma antioxidant potential and lowers plasma cholesterol levels. Clinica Chimica Acta, 284, 113–115. https://doi.org/10.1016/S0009-8981(99)00066-2
  • Edwards, K., Kwaw, I., Matud, J., Kurtz, I. (1999). Effect of Pistachio Nuts on Serum Lipid Levels in Patients with Moderate Hypercholesterolemia. Journal of the American College of Nutrition, 18(3), 229-232. https://doi.org/10.1080/07315724.1999.10718856
  • Fraser, G.E. (2000). Nut consumption, lipids, and risk of a coronary event. Asia Pacific Journal of Clinical Nutrition, 111, 11-15. https://doi.org/10.1046/j.1440-6047.2000.00181.x
  • Garner, B., Waldeck, A.R., Witting, P.K., Rye, K.-A., Stocker, R. (1998). Oxidation of high-density lipoproteins. II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins AI and AII. Journal of Biological Chemistry, 273 (13), 6088-6095. https://doi.org/10.1074/jbc.273.11.6088
  • Gießauf, A., Steiner, E., Esterbauer, H. (1995). Early destruction of tryptophan residues of apolipoprotein B is a vitamin E-independent process during copper-mediated oxidation of LDL. Biochimica et Biophysica Acta (BBA)/Lipids and Lipid Metabolism, 1256(2), 221–232. https://doi.org/10.1016/0005-2760(95)00024-7
  • Grundy, S.M., Cleeman, J.I., Bairey Merz, C.N., Brewer, H.B., Clark, L. T., Hunninghake, D.B., Pasternak, R.C., Smith, S.C., Stone, N.J. (2004). Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation,110, 227-239. https://doi.org/10.1161/01.CIR.0000133317.49796.0E
  • Hargrove, R.L., Etherton, T.D., Pearson, T.A., Harrison, E.H., Kris-Etherton, P.M. (2001). Low fat and high monounsaturated fat diets decrease human low density lipoprotein oxidative susceptibility in vitro. The Journal of Nutrition, 131(6), 1758–1763. https://doi.org/10.1093/jn/131.6.1758
  • Hasselwander, O., McEneny, J., McMaster, D., Fogarty, D.G., Nicholls, D.P., Maxwell, A.P., Young, I.S. (1999). HDL composition and HDL antioxidant capacity in patients on regular haemodialysis. Atherosclerosis, 143(1), 125-133. https://doi.org/10.1016/S0021-9150(98)00286-X
  • Jiang, R., Jacobs, D.R., Mayer-Davis, E., Szklo, M., Herrington, D., Jenny, N.S., Kronmal, R., Barr, R.G. (2006). Nut and seed consumption and inflammatory markers in the Multi-Ethnic Study of Atherosclerosis. American Journal of Epidemiology,163(3), 222-231. https://doi.org/10.1093/aje/kwj033
  • Kocyigit, A., Koylu, A.A., Keles, H. (2006). Effects of pistachio nuts consumption on plasma lipid profile and oxidative status in healthy volunteers. Nutrition, Metabolism and Cardiovascular Diseases, 16(3), 202–209. https://doi.org/10.1016/j.numecd.2005.08.004
  • Oliver H., Lowry, Nira J., Rosebrough A., Lewis Farr, Rose Randall (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry. 193 (1) 265-275. https://doi.org/10.1021/jf1005935. MercanlIgil, S.M., Arslan, P., Alasalvar, C., Okut, E., Akgül, E., PInar, A., Geyik, P.Ö., Tokgözoǧlu, L., Shahidi, F. (2007). Effects of hazelnut-enriched diet on plasma cholesterol and lipoprotein profiles in hypercholesterolemic adult men. European Journal of Clinical Nutrition. 61, 212-220. https://doi.org/10.1038/sj.ejcn.1602518
  • Mukuddem-Petersen, J., Oosthuizen, W., Jerling, J. C. (2005). A systematic review of the effects of nuts on blood lipid profiles in humans. The Journal of Nutrition, 135(9), 2082–2089. https://doi.org/10.1093/jn/135.9.2082
  • Nag, T., Ghosh, A. (2013). Cardiovascular disease risk factors in Asian Indian population: A systematic review. Journal of Cardiovascular Disease Research, 4 (4), 222-228. https://doi.org/10.1016/j.jcdr.2014.01.004
  • Negre-Salvayre, A., Dousset, N., Ferretti, G., Bacchetti, T., Curatola, G., Salvayre, R. (2006). Antioxidant and cytoprotective properties of high-density lipoproteins in vascular cells. Free Radical Biology and Medicine, 41(7), 1031-1040. https://doi.org/10.1016/j.freeradbiomed.2006.07.006
  • Nicholls, S.J., Nelson, A. J. (2019). HDL and cardiovascular disease. Pathology, 51(2), 142–147. https://doi.org/10.1016/j.pathol.2018.10.017
  • Norata, G.D., Pirillo, A., Catapano, A.L. (2006). Modified HDL: Biological and physiopathological consequences. Nutrition, Metabolism and Cardiovascular Diseases, 16(5), 371-386. https://doi.org/10.1016/j.numecd.2006.01.012
  • Öngün Yilmaz, H., Özyildirim, B. (2019). Evaluation of the effects of raisins and hazelnuts added to the diet on lipid profiles and anthropometric measurements in women with hyperlipidemia. Bezmialem Science, 7(4), 294–306. https://doi.org/10.14235/bas.galenos.2019.2969
  • Orem, A., Yucesan, F. B., Orem, C., Akcan, B., Kural, B. V., Alasalvar, C., Shahidi, F. (2013). Hazelnut-enriched diet improves cardiovascular risk biomarkers beyond a lipid-lowering effect in hypercholesterolemic subjects. Journal of Clinical Lipidology, 7(2), 123-131. https://doi.org/10.1016/j.jacl.2012.10.005
  • Proudfoot, J. M., Croft, K. D., Puddey, I. B., Beilin, L. J. (1997). The role of copper reduction by α-tocopherol in low-density lipoprotein oxidation. Free Radical Biology and Medicine, 23(5), 720-728. https://doi.org/10.1016/S0891-5849(97)00015-4
  • Puhl, H., Waeg, G., Esterbauer, H. (1994). Methods to determine oxidation of low-density lipoproteins. Methods in Enzymology, 233, 425-441 https://doi.org/10.1016/S0076-6879(94)33049-2
  • Renzo, L. Di, Cioccoloni, G., Bernardini, S., Abenavoli, L., Aiello, V., Marchetti, M., Cammarano, A., Alipourfard, I., Ceravolo, I., Gratteri, S. (2019). A hazelnut-enriched diet modulates oxidative stress and inflammation gene expression without weight gain. Oxidative Medicine and Cellular Longevity, 2019, 1-11. https://doi.org/10.1155/2019/4683723
  • Ros, E., Nunez, I., Perez-Heras, A., Serra, M., Gilabert, R., Casals, E., Deulofeu, R. (2004). A walnut diet improves endothelial function in hypercholesterolemic subjects: a randomized crossover trial. Circulation, 109(13), 1609-1614. https://doi.org/10.1161/01.CIR.0000124477.91474.FF
  • Garcı´a-L., I Megias R., J Salas S. (2003). Nut consumption and body weight. Am. J. Clinical Nutrition. 57(1), 8-11. https://doi.org/10.1038/sj.ejcn.1601802
  • Sclavons, M.M., Cordonnier, C.M., Mailleux, P.M., Heller, F.R., Desager, J.P., Harvengt, C.M. (1985). Fast separation of the three main plasma lipoprotein classes by ultracentrifugation using vertical rotor and multiple discontinuous density gradient. Clinica Chimica Acta, 153(2), 125-135. https://doi.org/10.1016/0009-8981(85)90163-9
  • Segovia-Siapco, G., Sabaté, J. (2018). Health and sustainability outcomes of vegetarian dietary patterns: a revisit of the EPIC-Oxford and the Adventist Health Study-2 cohorts. European Journal of Clinical Nutrition, 72, 60–70. https://doi.org/10.1038/s41430-018-0310-z
  • Singh, U.N., Kumar, S., Dhakal, S. (2017). Study of Oxidative Stress in Hypercholesterolemia. International Journal of Contemporary Medical Research, 4(5), 2454–7379.
  • Spiller, G.A., Gates, J.E., Cragen, L.N., Bruce, B., Jenkins, D.A.J., Bosello, O. (1998). Nuts and plasma lipids: An almond-based diet lowers LDL-C while preserving HDL-C. Journal of the American College of Nutrition, 17(3)-285-290. https://doi.org/10.1080/07315724.1998.10718761
  • Steinberg, D., Parthasarathy, S., Carew, T.E., Khoo, J.C., Witztum, J.L. (1989). Beyond cholesterol: Modifications of low-density lipoprotein that increase its atherogenicity. New England Journal of Medicine, 94, 215-244. Tey, S.L., Brown, R.C., Chisholm, A.W., Delahunty, C.M., Gray, A.R., Williams, S.M. (2011). Effects of different forms of hazelnuts on blood lipids and α-tocopherol concentrations in mildly hypercholesterolemic individuals. European Journal of Clinical Nutrition, 65, 117-124. https://doi.org/10.1038/ejcn.2010.200
  • Vanizor Kural, B., Örem, A., Çimşit, G., Yandı, Y.E., Calapoǧlu, M. (2003). Evaluation of the atherogenic tendency of lipids and lipoprotein content and their relationships with oxidant–antioxidant system in patients with psoriasis. Clinica Chimica Act, 328(1), 71-82. https://doi.org/https://doi.org/10.1016/S0009-8981(02)00373-X
  • Winklhofer-Roob, B.M., Faustmann, G., Roob, J.M. (2017). Low-density lipoprotein oxidation biomarkers in human health and disease and effects of bioactive compounds. Free Radical Biology and Medicine, 111, 38–86. https://doi.org/10.1016/j.freeradbiomed.2017.04.345
  • Zabłocka-Słowińska, K., Płaczkowska, S., Skórska, K., Prescha, A., Pawełczyk, K., Porębska, I., Kosacka, M., Grajeta, H. (2019). Oxidative stress in lung cancer patients is associated with altered serum markers of lipid metabolism. PLoS ONE, 14(4), 1–20. https://doi.org/10.1371/journal.pone.0215246

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research Articles
Authors

Buket AKCAN 0000-0002-4516-6528

Asım ÖREM 0000-0001-8450-5783

Birgül KURAL 0000-0003-0730-9660

Yahya ALTINKAYNAK 0000-0003-2060-4576

Fulya BALABAN YÜCESAN 0000-0002-9854-4721

Cihan ÖREM 0000-0001-6591-7336

Project Number 2007.114.01.4
Early Pub Date June 7, 2023
Publication Date July 5, 2023
Submission Date November 23, 2022
Published in Issue Year 2023Volume: 9 Issue: 3

Cite

APA AKCAN, B., ÖREM, A., KURAL, B., ALTINKAYNAK, Y., et al. (2023). Hazelnut-enriched diet effectively increases lipoproteins’ resistance to oxidation in hypercholesterolemic subjects. Food and Health, 9(3), 201-211. https://doi.org/10.3153/FH23019

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